Interpretive Summary: Scientists at the Center for Medical, Agricultural, and Veterinary Entomology, USDA-ARS, Gainesville, Florida describe here the results of a study aimed at determining how commonly, if ever, fire ant queens mate with more than one male. Our study revealed that some fire ant queens do indeed mate with more than one male and, unexpectedly, that whether a queen mates with more than a single male is determined almost entirely by male genotype. We also investigated the physiological basis for the inability of some males to discourage a second mating. We found that male sperm count is linked to male genotype as well, suggesting fire ant queens remain receptive to mating if their first partner does not provide a sufficient quantity of sperm. This study is groundbreaking by establishing how deleterious variation with respect to male fitness can be maintained as a consequence of being linked to genes harboring adaptive variation controlling social organization.

Technical Abstract:
Supergenes are groups of loci inherited together to facilitate the co-segregation of adaptive variation. We demonstrate that facultative polyandry and male reproductive success have a simple genetic basis in the fire ant Solenopsis invicta and depend solely on male genotype within the Gp-9 supergene. The associations of polyandry and male reproductive success with the Gp-9 supergene, which also controls social behavior in this ant, illustrate how selection acting to maintain variation for adaptive traits within a polymorphic supergene can simultaneously result in the maintenance of unfavorable variation affecting other traits.